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Parallel motion vision pathways in the brain of a tropical bee

Honkanen, Anna LU ; Hensgen, Ronja LU ; Kannan, Kavitha LU ; Adden, Andrea LU ; Warrant, Eric LU orcid ; Wcislo, William and Heinze, Stanley LU orcid (2023) In Journal of Comparative Physiology A: Neuroethology, Sensory, Neural, and Behavioral Physiology 209(4). p.563-591
Abstract

Spatial orientation is a prerequisite for most behaviors. In insects, the underlying neural computations take place in the central complex (CX), the brain’s navigational center. In this region different streams of sensory information converge to enable context-dependent navigational decisions. Accordingly, a variety of CX input neurons deliver information about different navigation-relevant cues. In bees, direction encoding polarized light signals converge with translational optic flow signals that are suited to encode the flight speed of the animals. The continuous integration of speed and directions in the CX can be used to generate a vector memory of the bee’s current position in space in relation to its nest, i.e., perform path... (More)

Spatial orientation is a prerequisite for most behaviors. In insects, the underlying neural computations take place in the central complex (CX), the brain’s navigational center. In this region different streams of sensory information converge to enable context-dependent navigational decisions. Accordingly, a variety of CX input neurons deliver information about different navigation-relevant cues. In bees, direction encoding polarized light signals converge with translational optic flow signals that are suited to encode the flight speed of the animals. The continuous integration of speed and directions in the CX can be used to generate a vector memory of the bee’s current position in space in relation to its nest, i.e., perform path integration. This process depends on specific, complex features of the optic flow encoding CX input neurons, but it is unknown how this information is derived from the visual periphery. Here, we thus aimed at gaining insight into how simple motion signals are reshaped upstream of the speed encoding CX input neurons to generate their complex features. Using electrophysiology and anatomical analyses of the halictic bees Megalopta genalis and Megalopta centralis, we identified a wide range of motion-sensitive neurons connecting the optic lobes with the central brain. While most neurons formed pathways with characteristics incompatible with CX speed neurons, we showed that one group of lobula projection neurons possess some physiological and anatomical features required to generate the visual responses of CX optic-flow encoding neurons. However, as these neurons cannot explain all features of CX speed cells, local interneurons of the central brain or alternative input cells from the optic lobe are additionally required to construct inputs with sufficient complexity to deliver speed signals suited for path integration in bees.

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author
; ; ; ; ; and
organization
publishing date
type
Contribution to journal
publication status
published
subject
keywords
Electrophysiology, Insects, Motion vision, Optic lobe, Path integration
in
Journal of Comparative Physiology A: Neuroethology, Sensory, Neural, and Behavioral Physiology
volume
209
issue
4
pages
563 - 591
publisher
Springer
external identifiers
  • pmid:37017717
  • scopus:85151491953
ISSN
0340-7594
DOI
10.1007/s00359-023-01625-x
language
English
LU publication?
yes
id
6833d0c5-3038-472c-9cb3-d3b6c50b2b8d
date added to LUP
2023-05-23 15:14:15
date last changed
2024-06-15 03:18:41
@article{6833d0c5-3038-472c-9cb3-d3b6c50b2b8d,
  abstract     = {{<p>Spatial orientation is a prerequisite for most behaviors. In insects, the underlying neural computations take place in the central complex (CX), the brain’s navigational center. In this region different streams of sensory information converge to enable context-dependent navigational decisions. Accordingly, a variety of CX input neurons deliver information about different navigation-relevant cues. In bees, direction encoding polarized light signals converge with translational optic flow signals that are suited to encode the flight speed of the animals. The continuous integration of speed and directions in the CX can be used to generate a vector memory of the bee’s current position in space in relation to its nest, i.e., perform path integration. This process depends on specific, complex features of the optic flow encoding CX input neurons, but it is unknown how this information is derived from the visual periphery. Here, we thus aimed at gaining insight into how simple motion signals are reshaped upstream of the speed encoding CX input neurons to generate their complex features. Using electrophysiology and anatomical analyses of the halictic bees Megalopta genalis and Megalopta centralis, we identified a wide range of motion-sensitive neurons connecting the optic lobes with the central brain. While most neurons formed pathways with characteristics incompatible with CX speed neurons, we showed that one group of lobula projection neurons possess some physiological and anatomical features required to generate the visual responses of CX optic-flow encoding neurons. However, as these neurons cannot explain all features of CX speed cells, local interneurons of the central brain or alternative input cells from the optic lobe are additionally required to construct inputs with sufficient complexity to deliver speed signals suited for path integration in bees.</p>}},
  author       = {{Honkanen, Anna and Hensgen, Ronja and Kannan, Kavitha and Adden, Andrea and Warrant, Eric and Wcislo, William and Heinze, Stanley}},
  issn         = {{0340-7594}},
  keywords     = {{Electrophysiology; Insects; Motion vision; Optic lobe; Path integration}},
  language     = {{eng}},
  number       = {{4}},
  pages        = {{563--591}},
  publisher    = {{Springer}},
  series       = {{Journal of Comparative Physiology A: Neuroethology, Sensory, Neural, and Behavioral Physiology}},
  title        = {{Parallel motion vision pathways in the brain of a tropical bee}},
  url          = {{http://dx.doi.org/10.1007/s00359-023-01625-x}},
  doi          = {{10.1007/s00359-023-01625-x}},
  volume       = {{209}},
  year         = {{2023}},
}